Wing patterning genes and coevolution of Müllerian mimicry inHeliconiusbutterflies: Support from phylogeography, cophylogeny, and divergence times

Examples of long-term coevolution are rare among free-living organisms. Müllerian mimicry in Heliconius butterflies had been suggested as a key example of coevolution by early genetic studies. However, research over the last two decades has been dominated by the idea that the best-studied comimics, H. erato and H. melpomene, did not coevolve at all. Recently sequenced genes associated with wing color pattern phenotype offer a new opportunity to resolve this controversy. Here, we test the hypothesis of coevolution between H. erato and H. melpomene using Bayesian multilocus analysis of five color pattern genes and five neutral genetic markers. We first explore the extent of phylogenetic agreement versus conflict between the different genes. Coevolution is then tested against three aspects of the mimicry diversifications: phylogenetic branching patterns, divergence times, and, for the first time, phylogeographic histories. We show that all three lines of evidence are compatible with strict coevolution of the diverse mimicry wing patterns, contrary to some recent suggestions. Instead, these findings tally with a coevolutionary diversification driven primarily by the ecological force of Müllerian mimicry

Measuring homoplasy I: comprehensive measures of maximum and minimum cost under parsimony across discrete cost matrix character types.

Here, we propose, prove mathematically and discuss maximum and minimum measures of maximum parsimony evolution across 12 discrete phylogenetic character types, classified across 4467 morphological and molecular datasets. Covered character types are: constant, binary symmetric, multistate unordered (non-additive) symmetric, multistate linear ordered symmetric, multistate non-linear ordered symmetric, binary irreversible, multistate irreversible, binary Dollo, multistate Dollo, multistate custom symmetric, binary custom asymmetric and multistate custom asymmetric characters. We summarize published solutions and provide and prove a range of new formulae for the algebraic calculation of minimum (m), maximum (g) and maximum possible (gmax) character cost for applicable character types. Algorithms for exhaustive calculation of m, g and gmax applicable to all classified character types (within computational limits on the numbers of taxa and states) are also provided. The general algorithmic solution for minimum steps (m) is identical to a minimum spanning tree on the state graph or minimum weight spanning arborescence on the state digraph. Algorithmic solutions for character g and gmax are based on matrix mathematics equivalent to optimization on the star tree, respectively for given state frequencies and all possible state frequencies meeting specified numbers of taxa and states. We show that maximizing possible cost (gmax) with given transition costs can be equivalent to maximizing, across all possible state frequency combinations, the lowest implied cost of state transitions if any one state is ancestral on the star tree, via the solution of systems of linear equations. The methods we present, implemented in the Claddis R package, extend to a comprehensive range, the fundamental character types for which homoplasy may be measured under parsimony using m, g and gmax, including extra cost (h), consistency index (ci), retention index (ri) or indices based thereon

Male and female contributions to diversity among birdwing butterfly images.

Machine learning (ML) newly enables tests for higher inter-species diversity in visible phenotype (disparity) among males versus females, predictions made from Darwinian sexual selection versus Wallacean natural selection, respectively. Here, we use ML to quantify variation across a sample of > 16,000 dorsal and ventral photographs of the sexually dimorphic birdwing butterflies (Lepidoptera: Papilionidae). Validation of image embedding distances, learnt by a triplet-trained, deep convolutional neural network, shows ML can be used for automated reconstruction of phenotypic evolution achieving measures of phylogenetic congruence to genetic species trees within a range sampled among genetic trees themselves. Quantification of sexual disparity difference (male versus female embedding distance), shows sexually and phylogenetically variable inter-species disparity. Ornithoptera exemplify high embedded male image disparity, diversification of selective optima in fitted multi-peak OU models and accelerated divergence, with cases of extreme divergence in allopatry and sympatry. However, genus Troides shows inverted patterns, including comparatively static male embedded phenotype, and higher female than male disparity - though within an inferred selective regime common to these females. Birdwing shapes and colour patterns that are most phenotypically distinctive in ML similarity are generally those of males. However, either sex can contribute majoritively to observed phenotypic diversity among species

Impacts of speciation and extinction measured by an evolutionary decay clock

The hypothesis that destructive mass extinctions enable creative evolutionary radiations (creative destruction) is central to classic concepts of macroevolution1,2. However, the relative impacts of extinction and radiation on the co-occurrence of species have not been directly quantitatively compared across the Phanerozoic eon. Here we apply machine learning to generate a spatial embedding (multidimensional ordination) of the temporal co-occurrence structure of the Phanerozoic fossil record, covering 1,273,254 occurrences in the Paleobiology Database for 171,231 embedded species. This facilitates the simultaneous comparison of macroevolutionary disruptions, using measures independent of secular diversity trends. Among the 5% most significant periods of disruption, we identify the ‘big five’ mass extinction events2, seven additional mass extinctions, two combined mass extinction–radiation events and 15 mass radiations. In contrast to narratives that emphasize post-extinction radiations1,3, we find that the proportionally most comparable mass radiations and extinctions (such as the Cambrian explosion and the end-Permian mass extinction) are typically decoupled in time, refuting any direct causal relationship between them. Moreover, in addition to extinctions4, evolutionary radiations themselves cause evolutionary decay (modelled co-occurrence probability and shared fraction of species between times approaching zero), a concept that we describe as destructive creation. A direct test of the time to over-threshold macroevolutionary decay4 (shared fraction of species between two times ≤ 0.1), counted by the decay clock, reveals saw-toothed fluctuations around a Phanerozoic mean of 18.6 million years. As the Quaternary period began at a below-average decay-clock time of 11 million years, modern extinctions further increase life’s decay-clock debt

Sclerite-bearing annelids from the lower Cambrian of South China

Cambrian annelids are strikingly diverse and reveal important details of annelid character acquisition. Their contribution, however, to a wider understanding of the evolution of the trochozoans (encompassing the annelids as well as such groups as the brachiopods and molluscs) remains limited. Thus the early annelids had been linked to a variety of cataphract Cambrian metazoans, notably Wiwaxia and the halkieriids, but recent work assigns such fossils to stem-group molluscs. Here we report two new annelids from the Lower Cambrian Chengjiang Lagerstätte, South China. Ipoliknus avitus n. gen., n. sp. is biramous with neurochaetae and notochaetae, but significantly also bears dorsal spinose sclerites and dorso-lateral dentate sclerites. Adelochaeta sinensis n. gen., n. sp. is unique amongst Cambrian polychaetes in possessing the rod-like supports of the parapodia known as aciculae. This supports phylogenetic placement of Adelochaeta as sister to some more derived aciculate Palaeozoic taxa, but in contrast Ipoliknus is recovered as the most basal of the stem-group annelids. Sclerites and chaetae of I. avitus are interpreted respectively as the remnants and derivatives of a once more extensive cataphract covering that was a characteristic of more primitive trochozoans. The two sets of chaetae (noto- and neurochaetae) and two sets of sclerites (spinose and dentate) suggest that in a pre-annelid an earlier and more complete scleritome may have consisted of four zones of sclerites. Other cataphract taxa from the Lower Palaeozoic show a variety of scleritome configurations but establishing direct links with such basal annelids as Ipoliknus at present must remain conjectural

Deep learning on butterfly phenotypes tests evolution’s oldest mathematical model

Traditional anatomical analyses captured only a fraction of real phenomic information. Here, we apply deep learning to quantify total phenotypic similarity across 2468 butterfly photographs, covering 38 subspecies from the polymorphic mimicry complex of Heliconius erato and Heliconius melpomene. Euclidean phenotypic distances, calculated using a deep convolutional triplet network, demonstrate significant convergence between interspecies co-mimics. This quantitatively validates a key prediction of Müllerian mimicry theory, evolutionary biology’s oldest mathematical model. Phenotypic neighbor-joining trees are significantly correlated with wing pattern gene phylogenies, demonstrating objective, phylogenetically informative phenome capture. Comparative analyses indicate frequency-dependent mutual convergence with coevolutionary exchange of wing pattern features. Therefore, phenotypic analysis supports reciprocal coevolution, predicted by classical mimicry theory but since disputed, and reveals mutual convergence as an intrinsic generator for the unexpected diversity of Müllerian mimicry. This demonstrates that deep learning can generate phenomic spatial embeddings, which enable quantitative tests of evolutionary hypotheses previously only testable subjectively

A possible Cambrian stem-group gnathiferan-chaetognath from the Weeks Formation (Miaolingian) of Utah

In recent years the plethora of “weird wonders”, the vernacular for the apparently extinct major bodyplans documented in many of the Cambrian Lagerstätten, has been dramatically trimmed. This is because various taxa have either been assigned to known phyla or at least accommodated in larger monophyletic assemblages. Nevertheless, a number of Cambrian taxa retain their enigmatic status. To this intriguing roster we add Dakorhachis thambus n. gen. n. sp., from the Miaolingian (Guzhangian) Weeks Formation Konservat-Lagerstätte of Utah. Specimens consist of an elongate body lacking appendages, but which is apparently segmented. A prominent feeding apparatus consists of a circlet of triangular teeth, while posteriorly there are three distinct skeletal components. D. thambus n. sp. is interpreted as an ambush predator and may have been partially infaunal. The wider affinities of this new taxon remain conjectural but it is suggested that it may represent a stem-group member of the Gnathifera, today represented by the gnathostomulids, micrognathozoans, rotifers, and possibly with links also to the chaetognaths

Phylogenetic Codivergence Supports Coevolution of Mimetic Heliconius Butterflies

The unpalatable and warning-patterned butterflies _Heliconius erato_ and _Heliconius melpomene_ provide the best studied example of mutualistic Müllerian mimicry, thought – but rarely demonstrated – to promote coevolution. Some of the strongest available evidence for coevolution comes from phylogenetic codivergence, the parallel divergence of ecologically associated lineages. Early evolutionary reconstructions suggested codivergence between mimetic populations of _H. erato_ and _H. melpomene_, and this was initially hailed as the most striking known case of coevolution. However, subsequent molecular phylogenetic analyses found discrepancies in phylogenetic branching patterns and timing (topological and temporal incongruence) that argued against codivergence. We present the first explicit cophylogenetic test of codivergence between mimetic populations of _H. erato_ and _H. melpomene_, and re-examine the timing of these radiations. We find statistically significant topological congruence between multilocus coalescent population phylogenies of _H. erato_ and _H. melpomene_, supporting repeated codivergence of mimetic populations. Divergence time estimates, based on a Bayesian coalescent model, suggest that the evolutionary radiations of _H. erato_ and _H. melpomene_ occurred over the same time period, and are compatible with a series of temporally congruent codivergence events. This evidence supports a history of reciprocal coevolution between Müllerian co-mimics characterised by phylogenetic codivergence and parallel phenotypic change

Australian spiny mountain crayfish and their temnocephalan ectosymbionts: an ancient association on the edge of coextinction?

Australian spiny mountain crayfish (Euastacus, Parastacidae) and their ecotosymbiotic temnocephalan flatworms (Temnocephalida, Platyhelminthes) may have co-occurred and interacted through deep time, during a period of major environmental change. Therefore, reconstructing the history of their association is of evolutionary, ecological, and conservation significance. Here, time-calibrated Bayesian phylogenies of Euastacus species and their temnocephalans (Temnohaswellia and Temnosewellia) indicate near-synchronous diversifications from the Cretaceous. Statistically significant cophylogeny correlations between associated clades suggest linked evolutionary histories. However, there is a stronger signal of codivergence and greater host specificity in Temnosewellia, which co-occurs with Euastacus across its range. Phylogeography and analyses of evolutionary distinctiveness (ED) suggest that regional differences in the impact of climate warming and drying had major effects both on crayfish and associated temnocephalans. In particular, Euastacus and Temnosewellia show strong latitudinal gradients in ED and, conversely, in geographical range size, with the most distinctive, northern lineages facing the greatest risk of extinction. Therefore, environmental change has, in some cases, strengthened ecological and evolutionary associations, leaving host-specific temnocephalans vulnerable to coextinction with endangered hosts. Consequently, the extinction of all Euastacus species currently endangered (75%) predicts coextinction of approximately 60% of the studied temnocephalans, with greatest loss of the most evolutionarily distinctive lineages

The Greatest Extinction Event in 66 Million Years? Contextualising Anthropogenic Extinctions

Biological communities are changing rapidly in response to human activities, with the high rate of vertebrate species extinction leading many to propose that we are in the midst of a sixth mass extinction event. Five past mass extinction events have commonly been identified across the Phanerozoic, with the last occurring at the end of the Cretaceous, 66 million years ago (Ma). However, life on Earth has always changed and evolved, with most species ever to have existed now extinct. The question is, are human activities increasing the rate and magnitude of extinction to levels rarely seen in the history of life? Drawing on the literature on extinctions primarily over the last 66 million years (i.e., the Cenozoic), we ask: (1) what comparisons can meaningfully be drawn? and (2) when did the Earth last witness an extinction event on this scale? We conclude that, although challenging to address, the available evidence suggests that the ongoing extinction episode still falls a long way short of the devastation caused by the bolide impact 66 Ma, but that it has likely surpassed most other Cenozoic events in magnitude, with the possible exception of the Eocene–Oligocene transition (34 Ma), about which much uncertainty remains. Given the number of endangered and at-risk species, the eventual magnitude of the current event will depend heavily on humanity's response and how we interact with the rest of the biosphere over the coming millennia